Relationships Between Gastrointestinal Parasite Infections and the Fecal Microbiome in Free-Ranging Western Lowland Gorillas

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2018 Jul 3

PMID 29963018

Citations 10

Authors

Klara Vlckova

Barbora Pafco

Klara J Petrzelkova

David Modry

Angelique Todd

Carl J Yeoman

Manolito Torralba

Brenda A Wilson

Rebecca M Stumpf

Bryan A White

Karen E Nelson

Steven R Leigh

Andres Gomez

Affiliations

Soon will be listed here.

Abstract

Relationships between gastrointestinal parasites (GIPs) and the gastrointestinal microbiome (GIM) are widely discussed topics across mammalian species due to their possible impact on the host's health. GIPs may change the environment determining alterations in GIM composition. We evaluated the associations between GIP infections and fecal microbiome composition in two habituated and two unhabituated groups of wild western lowland gorillas () from Dzanga Sangha Protected Areas, Central African Republic. We examined 43 fecal samples for GIPs and quantified strongylid nematodes. We characterized fecal microbiome composition through 454 pyrosequencing of the V1-V3 region of the bacterial 16S rRNA gene. spp. infections were associated with significant differences in abundances of bacterial taxa that likely play important roles in nutrition and metabolism for the host, besides being characteristic members of the gorilla gut microbiome. We did not observe any relationships between relative abundances of several bacterial taxa and strongylid egg counts. Based on our findings, we suggest that there is a significant relationship between fecal microbiome and infection in wild gorillas. This study contributes to the overall knowledge about factors involved in modulating GIM communities in great apes.

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References

Bracha R, Kobiler D, Mirelman D . Attachment and ingestion of bacteria by trophozoites of Entamoeba histolytica. Infect Immun. 1982; 36(1):396-406. PMC: 351231. DOI: 10.1128/iai.36.1.396-406.1982. View

Berg R . The indigenous gastrointestinal microflora. Trends Microbiol. 1996; 4(11):430-5. DOI: 10.1016/0966-842x(96)10057-3. View

Kreisinger J, Bastien G, Hauffe H, Marchesi J, Perkins S . Interactions between multiple helminths and the gut microbiota in wild rodents. Philos Trans R Soc Lond B Biol Sci. 2015; 370(1675). PMC: 4528493. DOI: 10.1098/rstb.2014.0295. View

Burgess S, Petri Jr W . The Intestinal Bacterial Microbiome and Infection. Curr Trop Med Rep. 2016; 3:71-74. PMC: 4967426. DOI: 10.1007/s40475-016-0083-1. View

Buffie C, Pamer E . Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013; 13(11):790-801. PMC: 4194195. DOI: 10.1038/nri3535. View

Wang J, Tang H, Zhang C, Zhao Y, Derrien M, Rocher E . Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J. 2014; 9(1):1-15. PMC: 4274436. DOI: 10.1038/ismej.2014.99. View

Seivwright L, Redpath S, Mougeot F, Watt L, Hudson P . Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol. 2004; 78(1):69-76. DOI: 10.1079/joh2003220. View

Koike S, Yoshitani S, Kobayashi Y, Tanaka K . Phylogenetic analysis of fiber-associated rumen bacterial community and PCR detection of uncultured bacteria. FEMS Microbiol Lett. 2003; 229(1):23-30. DOI: 10.1016/S0378-1097(03)00760-2. View

Mekonnen Z, Levecke B, Boulet G, Bogers J, Vercruysse J . Efficacy of different albendazole and mebendazole regimens against heavy-intensity Trichuris trichiura infections in school children, Jimma Town, Ethiopia. Pathog Glob Health. 2013; 107(4):207-9. PMC: 4001473. DOI: 10.1179/2047773213Y.0000000092. View

10.

Hayes K, Bancroft A, Goldrick M, Portsmouth C, Roberts I, Grencis R . Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science. 2010; 328(5984):1391-4. PMC: 3428897. DOI: 10.1126/science.1187703. View

11.

Cox F . History of human parasitology. Clin Microbiol Rev. 2002; 15(4):595-612. PMC: 126866. DOI: 10.1128/CMR.15.4.595-612.2002. View

12.

Slapeta J, Dowd S, Alanazi A, Westman M, Brown G . Differences in the faecal microbiome of non-diarrhoeic clinically healthy dogs and cats associated with Giardia duodenalis infection: impact of hookworms and coccidia. Int J Parasitol. 2015; 45(9-10):585-94. DOI: 10.1016/j.ijpara.2015.04.001. View

13.

. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486(7402):207-14. PMC: 3564958. DOI: 10.1038/nature11234. View

14.

Pafco B, cizkova D, Kreisinger J, Hasegawa H, Vallo P, Shutt K . Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci Rep. 2018; 8(1):5933. PMC: 5897349. DOI: 10.1038/s41598-018-24126-3. View

15.

Audebert C, Even G, Cian A, Loywick A, Merlin S, Viscogliosi E . Colonization with the enteric protozoa Blastocystis is associated with increased diversity of human gut bacterial microbiota. Sci Rep. 2016; 6:25255. PMC: 4857090. DOI: 10.1038/srep25255. View

16.

Ochman H, Worobey M, Kuo C, Ndjango J, Peeters M, Hahn B . Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 2010; 8(11):e1000546. PMC: 2982803. DOI: 10.1371/journal.pbio.1000546. View

17.

Tomkins A, Wright S, Drasar B, James W . Bacterial colonization of jejunal mucosa in giardiasis. Trans R Soc Trop Med Hyg. 1978; 72(1):33-6. DOI: 10.1016/0035-9203(78)90294-8. View

18.

Moeller A, Foerster S, Wilson M, Pusey A, Hahn B, Ochman H . Social behavior shapes the chimpanzee pan-microbiome. Sci Adv. 2016; 2(1):e1500997. PMC: 4730854. DOI: 10.1126/sciadv.1500997. View

19.

Morton E, Lynch J, Froment A, Lafosse S, Heyer E, Przeworski M . Variation in Rural African Gut Microbiota Is Strongly Correlated with Colonization by Entamoeba and Subsistence. PLoS Genet. 2015; 11(11):e1005658. PMC: 4664238. DOI: 10.1371/journal.pgen.1005658. View

20.

Nielsen M, Pfister K, von Samson-Himmelstjerna G . Selective therapy in equine parasite control--application and limitations. Vet Parasitol. 2014; 202(3-4):95-103. DOI: 10.1016/j.vetpar.2014.03.020. View